Data from the DARLING (Davis Area Research on Lactation, Infant Nutrition and Growth)
study were analyzed to determine whether the slower growth velocity of breast-fed infants
should be considered 'growth faltering' or is a normal outcome even under optimal
conditions. Anthropometry was completed monthly for 46 infants who were breast-fed for at
least 12 months. Energy intake was calculated from 4-day records of breast-milk and food
intake at 3, 6, 9 and 12 months. Morbidity was recorded weekly. Activity level was
assessed at 9 months by a 7-day sleep record and three 30-minute observations of
spontaneous activity while awake. At 3, 6, 9 and 12 months, gross energy intake averaged
569, 642, 738 and 844 kcal, or 91, 84, 87 and 92 kcal/kg, respectively. There was no
relationship between energy intake at any time point and morbidity during the subsequent
3-month period, nor between intake and activity level or time sleeping at 9 months.
Similarly, infants with slow growth velocity (below the 5th percentile) during each
quarter were just as healthy and active in the subsequent quarter as those with more rapid
growth. Preliminary data from a matched group of formula-fed infants show the expected
differences: higher energy intake and growth velocity, but no advantage in activity or
risk of illness. These results indicate that relatively low energy intakes and growth
velocities among breast-fed infants are normal patterns with no apparent deleterious
consequences in this population.

It has been documented that growth
patterns of breast-fed infants differ from those of formula-fed infants, upon whom most
reference data are based (WHITEHEAD and PAUL, 1981). The slower growth velocity of
breast-fed infants after the first 2-3 months has been called 'growth faltering' by some,
but it might just as easily be claimed that the growth pattern of formula-fed infants
represents 'excessive' growth. The problem is not just a semantic issue, however, as
evaluation of the health status of individual infants as well as groups of children
requires an appropriate standard. Historically, we have relied on growth measures as a
reflection of nutritional adequacy, but most would agree that bigger is not necessarily
better. What is needed, therefore, are alternative indices of functional outcomes to judge
whether a particular pattern of growth is optimal in a given environment.

The major objective of the DARLING
study was to assess growth and nutrient intake of breast-fed and formula-fed infants
during the first 18 months of life, and to include several functional indices, such as
morbidity and activity levels, which are then examined in relation to intake and growth
patterns. This paper presents an overview of the results pertaining to the breast-fed
cohort during the first 15 months. A more detailed description of methods and results will
be published elsewhere.

The study was designed to follow
prospectively 40-50 infants who were breast-fed for at least 12 months. This means that
breast milk was the sole source of milk, but other foods were introduced by parental
choice sometime after 4 months of age. Recruitment of a comparison group of formula-fed
infants, matching the breast-fed cohort, was begun in 1988. The sample population for both
groups was predominantly white, middle-to-upper income, highly educated women living in
the Davis, California area.

We recruited a total of 92 women who
intended to breast-feed for at least 12 months, of whom 73, 60, 51 and 46 remained in the
study at 3, 6, 9 and 23 months, respectively. Those who dropped out did so for primarily
two reasons, either because the infant stopped breast-feeding, or the study procedures
were no longer convenient, for instance because of changes in schedules or maternal
illness.

Home visits were conducted once a
month to measure both infant and mother and record infant feeding patterns. Infant
anthropometry included weight, length, arm and crown-rump lengths, head, arm, leg and
chest circumferences, and triceps, biceps, subscapular, flank and quadriceps skinfolds.

All mothers were contacted once a
week to record all symptoms of illness of the infant and mother. The nature and duration
of symptoms and any diagnoses made by physicians were noted. Morbidity data were
subsequently coded and grouped into four major categories: respiratory (coded as ill if
any upper or lower respiratory symptoms other than a clear nasal discharge were present),
diarrhea (defined as two or more runny stools per day that differed from the child's usual
stools), otitis media (diagnosed by a physician, with duration defined on the basis of
symptoms of fever or continued discomfort), and 'other' (unexplained fevers, vomiting,
chicken pox, and other non-respiratory, presumed viral infections). For the present
analysis, the total number of days ill with any illness, and by each category of illness,
was calculated in 3-month intervals: 0-3, 3-6, 6-9, 9-12 and 12-15 months. Incidence was
calculated as the number of episodes per 100 days at risk and is also presented as the
crude rate of episodes in each 3-month interval for convenience.

Infant intake was assessed at 3, 6,
9, 12, 15 and 18 months by having mothers complete a 4-day weighed record of all foods and
fluids. Breast-milk intake was determined by test-weighing, using a Sartorius 3826
(Brinkmann, Westbury, NY) electronic balance, accurate to the nearest gram and programmed
to average 40 consecutive weights, using an infant swing seat suspended from below for
older infants. All subjects were instructed to choose a 'typical' 4-day period for the
test-weighing record, i.e., days when the infant was not on an extended trip away from
home and had no overt symptoms of illness.

Because there is a systematic error
from test-weighing due to insensible water loss (IWL) during feedings, we corrected
breast-milk intake by estimating IWL for each infant. First, an adjustment factor was
determined by measuring IWL directly during both summer and winter months in a subsample
of infants. From a total of 342 measurements of 37 infants, an average loss of 0.05
g/kg/min was calculated, which was relatively constant from 3 to 12 months. This factor
was then multiplied by each infant's weight (in kilos) and by the total time of nursing
(in minutes) determined for each infant from the 4-day test-weighing record, and the
product (total IWL during feedings, in grams) was added to the breast-milk intake measured
by test-weighing.

Samples of human milk representative
of a 24-hour period were collected from each mother after the 4-day test-weighing period,
using the alternate breast-expression method (BUTTE et al., 1984). Milk was
analyzed for protein by a modified Lowry technique (PETERSON, 1977), fat by the modified
Folch extraction procedures (FOLCH et al., 1957; FERRIS and JENSEN, 1984), and
lactose by the method described by DAHLQUIST (1964). Gross energy content was calculated
from values for protein, fat and lactose using the factors of 5.65, 9.25 and 3.95 kcal/g,
respectively (GARZA et al., 1985). Gross energy intake of infants was calculated by
multiplying the gross energy density of their mothers' milk by the corrected breast-milk
intake, and adding energy from other foods using the factors of 9.4 kcal/g for fat, 5.65
kcal/g for protein, and 4.15 kcal/g for carbohydrate (PIKE and BROWN, 1984).

At 9 and 18 months of age, infant
activity level was assessed in two ways: (1) by having the mother record all time that her
infant spent sleeping on seven consecutive days, and (2) by observation of each infant for
30 minutes on three separate days. The 7-day record was used to obtain an overall picture
of time awake vs time asleep, while the second method was chosen to reflect spontaneous
activity level of infants while awake. The latter procedure was adapted from an activity
assessment method for preschool children developed by KLESGES et al. (1984). A
trained assistant went to the home at a time when the infant was healthy, rested and
recently fed to observe it for 30 minutes. Mothers were instructed not to hold or
constrain the child more than necessary so that the infant's voluntary level of physical
activity could be observed. After the infant became accustomed to the presence of the
observer, recording was begun using a standardized form. During the 30-minute period,
activity was observed for 10 seconds, then recorded for 10 seconds alternately for a total
of 90 ratings each time. Activity was recorded by six categories of behavior (lying down,
sitting supported, sitting unsupported, creeping, crawling and cruising/walking), each
with three levels of movement, for a total of 18 subcategories. A score was calculated,
based on time spent in each subcategory, and averaged over the three days of observation.
Further details of this method and the scoring system utilized are available from the
authors on request.

Data were analyzed using the
Statistical Package for the Social Sciences (1983). Energy intake data for infants whose
mothers had difficulty with either the test-weighing record or the milk sample collection
procedure were excluded from analysis. Several methods were used to determine whether the
outcome measures of morbidity and activity showed any relationship to prior energy intake
or growth velocity. First, simple correlation analysis and inspection of scatterplots were
used to examine whether any trends were evident, and if so, whether the relationships were
linear or non-linear. Second, at each time point, infants were divided into groups with
lower versus higher energy intake (divided at the median) and lower versus higher growth
velocity (divided at the 5th percentile of recent data published by ROCHE et al.
(1989)). Both parametric (Student's t-tests) and non-parametric (Mann-Whitney U-tests)
methods were used to compare subsequent morbidity and activity of groups, as some of the
dependent variables were highly skewed. Analysis of variance and multiple regression were
then used to control for potentially confounding variables in the morbidity comparisons,
such as season, time spent in day care, sex, and socioeconomic status. Because there were
only two mothers in the breast-fed cohort who smoked, this variable could not be included
in the analysis.

Breast-milk intake, corrected for
insensible water loss, averaged 813, 769, 637 and 445 g/d at 3, 6, 9 and 12 months,
respectively, with the corresponding gross energy densities of milk being 70.2, 71.8, 74.2
and 73.7 kcal/100 9. Gross energy intakes, including both breast milk and other foods
after 4 months of age, are shown in Table 1, with preliminary data for the
formula-fed group shown for comparison. The percentage of energy intake contributed by
breast milk averaged 100% at 3 months, 86% at 6 months, 65% at 9 months, and 39% at 12
months.

Total energy intake of breast-fed
infants increased steadily from 3 to 12 months, but was significantly lower than that of
formula-fed infants at all time points, even though neither group started to consume solid
foods until 4 months of age or later. When expressed as intake per kg, average values for
breast-fed infants reached a nadir of 84.1 kcal/kg at 6 months, and were far below the
current RDA (Food and Nutrition Board, 1989) of 108 kcal/kg from 1 to 6 months and 98
kcal/kg from 6 to 12 months, despite the fact that the latter values are for metabolizable
energy intake, and our data are for gross energy intake. Intake per kg of breast-fed
infants differed significantly from that of formula-fed infants at 3, 6 and 9 months.

Growth patterns of the breast-fed
cohort also differ from current NCHS reference data, with high Z-scores for weight-forage
initially, because of the high mean birthweight (3685 ±508 9), dropping off to Z (0 at
6-7 months and further declining to Z (-0.4 at 10-12 months (DEWEY et al., 1989).
Length-for-age Z-scores show the same initial pattern but do not remain below the NCHS
median after 8 months of age. The relative decline in weight-for-age is not merely an
artifact of the high mean birthweight, as the same slope is observed when only the average
birthweight infants are included in the plot (DEWEY et al., 1989). Preliminary data
for the formula-fed group do not show the relative decline observed in the breast-fed
cohort.

When presented as growth-velocity
data, the difference between the breast-fed group and current reference data is even more
apparent. Table 2 lists the number of breast-fed infants with velocities below the
5th percentile of recently published data from the Fels Longitudinal Study (ROCHE et al.,
1989). The percentage of infants falling below this cut-off for weight gain ranged from
20% at 0-3 months to 52% at 9-12 months. Similar percentages were observed for length gain
below the 5th percentile. Although expressing the data in this way is useful for
comparative purposes, it should be recognized that the percentiles published are based on
smoothed growth curves for each infant in the Fels data set. Because infant growth occurs
in spurts, using actual increments rather than estimated increments would result in a
wider distribution and hence more individuals falling below the Fels 5th percentile.

Descriptive data on morbidity in the
breast-fed cohort are shown in Table 3. Infants were ill an average of 7.5 days
during the first trimester, and about 20 days per trimester from 6 to 15 months of age.
The vast majority of illnesses were respiratory, with a very low prevalence of diarrhea!
disease in this population. Preliminary data for the formula-fed group indicate that
overall morbidity rates are similar to those observed in the breast-fed group.

Table 3. Morbidity data for
breast-fed infants

Age range (mo)

0-3

3-6

6-9

9-12

12-15

n

72

66

58

47

45

Mean number of days ill

Total

7.2

16.7

21.7

18.7

19.1

Respirator

6.3

15.9

18.2

14.0

13.5

Diarrhea

0.3

0.2

0.8

1.9

3.0

Otitis

0.3

1.2

2.5

2.9

2.1

Other

0.2

0.7

1.2

2.0

2.3

Mean number of episodes

Total

0.9

2.0

2.6

2.7

3.1

Respiratory

0.8

1.6

1.7

1.4

1.7

Diarrhea

0.04

0.08

0.17

0.26

0.49

Otitis

0.04

0.23

0.43

0.49

0.29

Other

0.06

0.15

0.28

0.53

0.62

Time sleeping at 9 months ranged
from 9.8 to 14.8 hours, with an average of 12.0 ±1.0 for boys and 12.2 ±1.1 for girls.
Activity scores ranged from 312 to 435, with an average of 384 ±27 for boys and 387 ±27
for girls. Preliminary data for the formula-fed group showed no differences in time
sleeping or activity level when compared to the breast-fed group.

Regression analysis at each time
point (3, 6, 9 and 12 months) showed no relationship between energy intake, either total
intake or intake per kg, and total morbidity during the subsequent 3-month period, whether
morbidity was expressed as total number of days ill (prevalence), incidence, or duration
of episodes. Similarly, activity score and time sleeping were not related to energy intake
or intake per kg at 9 months. When infants were divided into lower versus higher energy
intake groups, again no differences were seen in morbidity or activity at any time point.

The same results were found when
comparing morbidity and activity of infants with slow growth velocity: infants whose
weight or length gain fell below the 5th percentile were not different in activity or
subsequent morbidity from infants with higher growth velocities.

(a) Energy intake of breast-fed infants is far below current recommended levels
throughout the first year of life, even in a population of well-nourished, high
socioeconomic status families and with complementary feeding after 4-6 months. We have
shown previously that these low intakes are due more to infant self-regulation of intake
than to constraints on maternal breast-milk production (DEWEY and LÖNNERDAL, 1986).
Furthermore, infants provided with solid foods tend to reduce their intake of breast milk
initially, rather than increasing energy intake, indicating that they do not consume all
of the energy made available to them (STUFF and NICHOLS, 1989; NOMMSEN et al.,
1989).

(b) Growth velocity of breast-fed
infants is also considerably lower than current reference data, even as late as 9-12
months of age when other foods provide the majority of the child's energy intake. However,
differences in achieved growth by 12 months of age are apparent only for weight, not for
length, indicating that, on the average, these infants are leaner but not shorter than the
NCHS median.

(c) Morbidity, time sleeping, and
activity are unrelated to low energy intake or slow growth velocity in our cohort of
breast-fed infants. In other words, infants with low intakes and slow growth were just as
healthy and active as infants with higher intakes and more rapid growth. Thus, the
deviation of breast-fed infants from current recommendations for energy intake and growth
can be considered a normal pattern with no apparent deleterious consequences in our
population. Further research is necessary to establish guidelines for identifying truly
inadequate intakes and growth faltering among breast-fed infants in different
environments.